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Phylogeny and Circumscription of Sapindaceae Revisited: Molecular Sequence Data, Morphology and Biogeography Support Recognition of a New Family, Xanthoceraceae

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Phylogeny and Circumscription of Sapindaceae Revisited: Molecular Sequence Data, Morphology and Biogeography Support Recognition of a New Family, Xanthoceraceae Plant Ecology and Evolution 143 (2): 148–159, 2010 doi:10.5091/plecevo.2010.437 REGULAR PAPER Phylogeny and circumscription of Sapindaceae revisited: molecular sequence data, morphology and biogeography support recognition of a new family, Xanthoceraceae Sven Buerki1, Porter P. Lowry II2,3,*, Nadir Alvarez4, Sylvain G. Razafimandimbison5, Philippe Küpfer6 & Martin W. Callmander2,7 1Department of Biodiversity and Conservation, Real Jardin Botanico, CSIC, Plaza de Murillo 2, ES-28014 Madrid, Spain 2Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, U.S.A. 3Muséum National d’Histoire Naturelle, Case Postale 39, 57 rue Cuvier, FR-75231 05 CEDEX, Paris, France 4Department of Ecology and Evolution, Biophore, University of Lausanne, CH-1015 Lausanne, Switzerland 5Department of Botany, Bergius Foundation, SE-10691, Stockholm University, Stockholm, Sweden 6Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, CH-2000 Neuchâtel, Switzerland 7Conservatoire et Jardin botaniques de la ville de Genève, ch. de l’Impératrice 1, CH-1292 Chambésy, Switzerland *Author for correspondence: [email protected] Background and aims – Recent studies have adopted a broad definition of Sapindaceae that includes taxa traditionally placed in Aceraceae and Hippocastanaceae, achieving monophyly but yielding a family difficult to characterize and for which no obvious morphological synapomorphy exists. This expanded circumscription was necessitated by the finding that the monotypic, temperate Asian genus Xanthoceras, historically placed in Sapindaceae tribe Harpullieae, is basal within the group. Here we seek to clarify the relationships of Xanthoceras based on phylogenetic analyses using a dataset encompassing nearly ¾ of sapindaceous genera, comparing the results with information from morphology and biogeography, in particular with respect to the other taxa placed in Harpullieae. We then re-examine the appropriateness of maintaining the current broad, morphologically heterogeneous definition of Sapindaceae and explore the advantages of an alternative family circumscription. Methods – Using 243 samples representing 104 of the 142 currently recognized genera of Sapindaceae s. lat. (including all in Harpullieae), sequence data were analyzed for nuclear (ITS) and plastid (matK, rpoB, trnD-trnT, trnK-matK, trnL-trnF and trnS-trnG) markers, adopting the methodology of a recent family- wide study, performing single-gene and total evidence analyses based on maximum likelihood (ML) and maximum parsimony (MP) criteria, and applying heuristic searches developed for large datasets, viz. a new strategy implemented in RAxML (for ML) and the parsimony ratchet (for MP). Bootstrap analyses were performed for each method to test for congruence between markers. Key results – Our findings support earlier suggestions that Harpullieae are polyphyletic: Xanthoceras is confirmed as sister to all other sampled taxa of Sapindaceae s. lat.; the remaining members belong to three other clades within Sapindaceae s. lat., two of which correspond respectively to the groups traditionally treated as Aceraceae and Hippocastanaceae, together forming a clade sister to the largely tropical Sapin- daceae s. str., which is monophyletic and morphologically coherent provided Xanthoceras is excluded. Conclusion – To overcome the difficulties of a broadly circumscribed Sapindaceae, we resurrect the his- torically recognized temperate families Aceraceae and Hippocastanaceae, and describe a new family, Xan- thoceraceae, thus adopting a monophyletic and easily characterized circumscription of Sapindaceae nearly identical to that used for over a century. Key words – Aceraceae, Harpullieae, Hippocastanaceae, molecular phylogeny, new family, Sapindaceae, Xanthoceras, Xanthoceraceae. All rights reserved. © 2010 National Botanic Garden of Belgium and Royal Botanical Society of Belgium – ISSN 2032-3913 Buerki et al., Recognition of a new family, Xanthoceraceae INTRODUCTION and include both evergreen and deciduous species (Radlkofer 1933, Müller & Leenhouts 1976). Based on wood anatomy, The systematics of the family Sapindaceae has challenged Klaassen (1999) noted a difference between the temperate taxonomists for more than a century since its first compre- and tropical genera in the tribe, and among the tropical ones hensive treatment was published by Radlkofer (1890, 1933). he indicated that Delavaya and Ungnadia stood out because Until the late 1980s, Sapindaceae were widely treated as their wood is similar to that of members of tribe Cupanieae distinct from two closely related families, Hippocastanaceae Reichenb. (Sapindoideae). Buerki et al. (2009) found Harpul- and Aceraceae, based primarily on morphology and bioge- lieae to be polyphyletic, with Xanthoceras occupying a basal ography (Takhtajan 1987, Cronquist 1988, Dahlgren 1989). position within Sapindaceae s. lat., Arfeuillea, Eurycorymbus, Several recent studies using pollen morphology (Müller & Harpullia and Majidea placed in Dodonaeoideae, Delavaya Leenhouts 1976), phytochemistry (Umadevi & Daniel 1991) occupying a basal position within Sapindoideae, and Concho- and molecular sequence data (Gadek et al. 1996, Savolainen petalum resolved in the Macphersonia group (Sapindoideae; et al. 2000, APG II 2003, APG III 2009, Harrington et al. Buerki et al. 2009) closely related to the newly described en- 2005, Buerki et al. 2009) have, however, led to the adoption demic Malagasy genus Gereaua Buerki & Callm. (Buerki et al. of a broader concept in an effort to ensure monophyly, uniting 2010). A close relationship between Delavaya and Ungnadia these entities into a single family, Sapindaceae s. lat. was found in an earlier cladistic analysis based on morphol- Sapindaceae s. lat. as currently circumscribed by Har- ogy (Judd et al. 1994), which identified the presence of pro- rington et al. (2005), Thorne & Reveal (2007) and Buerki longed basal petal appendages and glabrous stamens as puta- et al. (2009, 2010) comprise c. 1900 species and 142 genera tive synapomorphies, again suggesting that Harpullieae were distributed among four subfamilies: Dodonaeoideae Burnett, far from representing a natural assemblage. Hippocastanoideae Burnett, Sapindoideae Burnett and Xan- In the present study we seek to (1) clarify the relation- thoceroideae Thorne & Reveal. Recently, Buerki et al. (2009) ships of Xanthoceras within Sapindaceae s. lat. and in particu- demonstrated the para-/polyphyly of all tribes as defined by lar with respect to the other taxa traditionally and/or currently Radlkofer (1933), with a single exception, Paullinieae Kunth. placed in Harpullieae, and (2) re-examine the appropriateness Although they sketched an informal system that recognizes a of maintaining the current broadly circumscribed but mor- dozen monophyletic groups, they did not propose new tribal phologically heterogeneous definition of Sapindaceae and limits within the four subfamilies as many potentially impor- explore the possible advantages of alternative family circum- tant genera of Sapindaceae were not included in their study scriptions. Toward this end, we have significantly expanded due to the lack of sequenceable material. the dataset of Buerki et al. (2009) to conduct a new set of Historically, Radlkofer (1933) recognized fourteen tribes phylogenetic analyses, comparing the results with informa- within Sapindaceae s. str., five in Dodonaeoideae and nine in tion from morphology and biogeography. Sapindoideae (see table 1 in Buerki et al. 2009 for details). Within Dodonaeoideae, however, he encountered difficulty MATERIAL AND METHODS assigning nine genera to the four previously described tribes, ultimately deciding to place them in a new tribe, Harpullieae Sampling, sequence data and phylogenetic analyses Radlk. Within this heterogeneous assemblage, he recognized two informal groups according to the presence (Delavaya Fran- Species names, voucher information, and GenBank accession chet, Ungnadia Endl. and Xanthoceras Bunge) or absence (Ar- numbers for all sequences are provided in the appendix. The feuillea Pierre, Conchopetalum, Eurycorymbus Hand.-Mazz., dataset presented in Buerki et al. (2009) was expanded to in- Harpullia Roxb., Magonia A.St.-Hil. and Majidea J.Kirk ex clude a total of 243 samples encompassing more than 70% of Oliv.) of a terminal leaflet. While revising Radlkofer’s infra- the generic diversity in Sapindaceae s. lat. (104 of the currently familial system, largely on the basis of pollen and other mor- recognized 142 genera; half of the 38 genera not included in phological features, Müller & Leenhouts (1976) discussed the this analysis are monospecific), representing an increase of possible expansion of Harpullieae to include the three genera ninety ingroup samples and nineteen genera. To assess the phy- comprising Hippocastanaceae, viz. Aesculus L., Billia L. and logenetic relationships of the taxa placed in tribe Harpullieae Handeliodendron (these authors did not, however, comment on and in the traditionally recognized families Aceraceae and Hip- the taxonomic status of Aceraceae). In their revised classifica- pocastanaceae, we sampled at least one species from each ge- tion, Müller & Leenhouts (1976) concluded that the connection nus currently assigned to these groups by adding the following between Hippocastanaceae and Harpullieae might involve two genera: Magonia and Ungnadia from Harpullieae, plus Billia genera in particular, Handeliodendron, originally described in and Handeliodendron from Hippocastanaceae (Aesculus, the
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